Carabid Beetle Assemblages in Three Environments in the Araucaria Humid Forest of Southern Brazil

Revista Brasileira de Entomologia http://dx.doi.org/10.1590/S0085-56262013000100011

Carabid beetle assemblages in three environments in the Araucaria humid forest of southern Brazil

Rodrigo Milton Moraes1,2, Milton de Souza Mendonça Jr1 & Ricardo Ott2

1Laboratório de Ecologia de Interações, Departamento de Ecologia, Instituto de Biologia, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves, 9500, 91501–970 Porto Alegre-RS, Brazil. [email protected] 2Museu de Ciências Naturais, Fundação Zoobotânica do Rio Grande do Sul, Av. Salvador França, 1427, 90690–000 Porto Alegre-RS, Brazil. [email protected]

ABSTRACT. Carabid beetle assemblages in three environments in the Araucaria humid forest of southern Brazil. Carabidae is composed mainly by ground-dwelling predator beetles. It is the fourth most diverse group within Coleoptera, but its diversity in the Neotropical region is understudied. Here we describe and analyze the diversity of carabid beetles in a region of subtropical rain forest dominated by Araucaria angustifolia with different landscapes. Three areas were chosen in an environmental integrity gradient: primary forests, secondary forests and old Pinus plantations. Pitfall traps were taken monthly, in a total of 14 samples per area. 1733 adult carabid beetles, belonging to 18 species, were sampled. There were differences in richness and abundance between the sampled areas. The total scores followed the same tendency: primary forests (14 species/747 individuals), secondary forests (13/ 631) and Pinus forests (10/355). An analysis of similarity shows differences in species composition, for both areas and seasons. Galerita lacordarei was the most abundant species for all samples and seasons. Carabid species show similar responses in accordance with habitat heterogeneity and disturbance. The abundance of Galerita lacordarei was influenced by temperature, for all sampled sites. Environmental changes affect the carabid assemblages and decrease diversity, possibly interfering in local dynamics. Seasonality patterns seem to indicate an increase in individual movement during summer, probably in search of resources. It is suggested that microhabitat patchiness is probably an important factor affecting carabid beetle diversity at small spatial scales.

KEYWORDS. Carabidae; Coleoptera; diversity; Insecta; pitfall trap.

Carabids are typical soil beetles, usually found on sandy agroecosystems (Thomas et al. 2006; Boivin & Hance 2002; terrain, under rocks and litter (Triplehorn & Johnson 2005), Melnychuk et al. 2003; Jukes et al. 2001; Holland & Luff but some groups inhabit trees and shrubs (Erwin 2000). Ac- 2000; Tonhasca 1994). Some of these studies relate the cara- cording to Marinoni et al. (2001) and Marinoni (2001), carabid fauna to environmental variables (e.g. temperature, rain- bids are included in the carnivore trophic group given their fall, canopy cover, soil organic matter content, etc). predatory character. However, some are specialised in feed- Nevertheless, we do not know which of these variables best ing on fruits and seeds (Paarmann et al. 2001, 2002). correlate to observed patterns of richness and abundance This family is estimated to be the fourth largest group in (Niemelä 1996) and which are more informative at a certain Coleoptera, with approximately 40,000 species (Bouchard scale and/or situation (e.g. preserved x altered environments). et al. 2009). In the Neotropical region, Reichardt (1979) es- Work on the diversity and dynamics of carabid assemblages timated 4,400 species grouped in 330 genera and Roig-Juñent show clear trends. Although heterogeneous environments have (1998) put these numbers at 194 genera for Brazil. Reichardt higher diversity and abundance (Fujita et al. 2008; Hartley et (1977) cited for Brazil the greatest part of the known carabid al. 2007; Magura et al. 2003; Butterfield 1997), when the cara- richness for the Neotropics, mainly concentrated in the tropi- bid fauna is compared between undisturbed and disturbed en- cal forests (Arndt et al. 2005). This information can only vironments, richness appears to be higher in the latter. This bring an approximation given the present lack of carabid spe- can be a consequence of generalist species emigrating from cialists and the historically conflicting taxonomy of this group open areas, given the appropriate conditions created by distur- especially for the tropics (Ball 1996). bance (Latty et al. 2006). In some of these cases, abundance Studies in carabids have addressed their diversity through can be also higher (Uehara-Prado et al. 2009). Carabid spe- distinct themes: successional stages (Tyler 2008; Magura et cies composition changes under structural changes of the habi- al. 2003; Humphrey et al. 1999); fragmentation and tat (Scott & Anderson 2003), being perhaps one of the most urbanisation (Fujita et al. 2008; Hartley et al. 2007; Lövei et informative ways of studying faunal variations (Penev 1996). al. 2003); disturbance gradients (Silva et al. 2008); responses Some subtropical assemblages seem to have at least one domi- to environmental characteristics (Uehara-Prado et al. 2009; nant species (Moura 2007), sometimes varying among envi- Schreiner & Irmler 2009; Latty et al. 2006; Fernández & ronments (Werner & Raffa 2000). Within habitat, small-scale Costas 2004; Larsen & Work 2003; Werner & Raffa 2000); influences (e.g. “patchiness”), are cited as determinant for the regeneration in natural areas (Ings & Hartley 1999) and local diversity of Carabidae (Schreiner & Irmler 2009).

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Carabids are increasingly being used as bioindicators of maintained conservation unit is at a crossroads between the environmental integrity. Taylor & Dorann (2001), for ex- Basaltic Highlands and Coastal Plain regions, in an area of ample, suggest monitoring the effectiveness of restoring al- considerable rainfall (annual average higher than 1,800 mm). tered areas using this group as indicator. In order to foster The average annual temperature is 16ºC, with average maxi- and widen such uses it is important to understand the pat- mum and minimum at 27ºC and 6ºC, respectively. Jungblut & terns shown by carabid populations in differing environments Pinto (1997) highlight the soil humidity as a function of con- of the Neotropical region. Thus it is necessary to couple bio- tinuous rains, with no dry season. logical and ecological work on this group. Bohac (1999) also Three forest environments were chosen for comparison: suggests that studying carabids along with other edaphic primary forest, secondary forest and an area under silvicul- arthropods (as staphilinids and arachnids) would enhance our ture with Pinus spp. The primary forest has a predominance of knowledge on soil responses to human change. This has been Araucaria angustifolia (Bertol.) Kuntze composing the top done in Europe (Desender et al. 1991) and North America canopy layer, the tree stratum is high, with a shrub stratum (Rainio & Niemelä 2003; Brown 1997; Eyre et al. 1996), but formed by smaller trees and sparse bamboo clumps. The secon- again such studies are lacking in the Neotropics so far. dary forest has an abundance of Tibouchina sellowiana (Cham.) Among researches using coleopterans for biodiversity stud- Cogn, the shrub layer is less expressive, and bamboo clumps ies in the Neotropics, few consider the Carabidae family alone. are very frequent. Silviculture areas maintain populations of Sampling in South America by Erwin (1990), Lucky et al. exotic Pinus taeda L. and Pinus elliotti Engelm. planted de- (2002) and Erwin et al. (2005) investigated the diversity of cades ago, which explains the presence of a shrub layer com- forest canopy carabids in the Amazon. The latter two studies posed of young native trees besides its characteristic and highlight the strong influence that microhabitats can have on compact litter. These environments represent a disturbance gra- the carabidofauna. Erwin (1990) describes the characteristics dient: the primary forest has been minimally disturbed, the composing such microhabitats and emphasises the importance secondary forest historically suffered some disturbance due to of environmental complexity for carabid diversity. selective logging and Pinus spp. silviculture areas are highly Studies developed in Brazil include those of Adis et al. disturbed, although a long time has passed allowing a partial (1986, 1990, 1997), gathering data on the diversity and biol- recovery of the local flora and fauna. ogy of carabids in the Amazon; Vieira (2008) examined forest Each environment had two replicate sampling sites, each fragments in the Pantanal; Martins et al. (2009) investigated site receiving 10 pitfall traps, 10 m far from each other and carabid population fluctuations in an agroecosystem at the organized in two transects. The trap was built from a 500 ml interface between crops of soybean and of maize. Aspects of plastic cup (10 cm diameter, 15 cm depth). Traps were cove- the Amazonian carabid guilds dynamics were also described red 10 cm above the cup border to avoid overflowing with by Paarmann et al. (2001, 2002). rain. Preserving liquid was formaldehyde 4% with added de- Experiments in exotic silviculture reveal a low diversity tergent drops to reduce surface tension. Traps were removed for carabids (Holtz et al. 2001), without significant change and changed every 30 days, operating from February 2001 across seasons in the subtropics (Soares & Costa 2001). Some until April 2002. Fourteen samples were obtained per site. implications of the presence of silviculture environments on The carabid specimens were sorted out from samples car- the beetle fauna in southern Brazil are discussed in Ganho & ried out in the study of Ott (2004), with the remaining mate- Marinoni (2006) (for other predatory invertebrate group rial being stored in Museu de Ciências Naturais, FZB-RS. The (arachnids) see Baldissera et al. 2008). carabid beetles were identified with help of taxonomic sources The diversity of carabid beetles in Rio Grande do Sul (Reichardt 1967, 1977). A reference collection was established state is little explored except for Diefenbach & Becker (1992a, with specimens deposited at “Museu de Ciências Naturais” of b), which sampled an urban park with pitfalls, especially in FZB-RS, Porto Alegre, documented through digital images. places covered with exotic ivy (Hedera helix, Araliaceae). Environments and climatic seasons were the two factors This last work revealed a seasonal cycle for carabids species used in statistical analysis. To test for differences in species in this region. Moura (2007) considered the diversity of cara- richness (species density sensu Gotelli & Colwell 2001), bids among regions of the coastal plain. sample-based rarefactions for the two factors were imple- Our aim is to compare the diversity of carabid assem- mented in PASt software (Hammer et al. 2001). To test for blages among distinct forest formations (both natural and the effect distance between sampling areas has over the com- artificial) in the Araucaria humid forest ecoregion, Rio position of the carabid fauna a Mantel test was used, con- Grande do Sul state, also investigating the influence that tem- fronting a geographical between-transect distance matrix with perature and rainfall can have on this fauna. a composition similarity matrix (both Simpson and Morisita indexes, also in PASt). To compare three related diversity MATERIAL E METHODS variables simultaneously (abundance, species richness and equitability) we employed a two-factor MANOVA in SPSS Sampling took place at the Centro de Pesquisa e Conserva- 16.0. Species composition was tested with four ANOSIM ção da Natureza Pró-Mata, in São Francisco de Paula munici- (Analysis of Similarity) tests, for both factors and two simi- pality, Rio Grande do Sul, in southern Brazil. This privately larity indexes, a qualitative (Simpson) and a quantitative one

Revista Brasileira de Entomologia 57(1): 67–74, March 2013 Carabid beetle assemblages in three environments in the Araucaria humid forest of southern Brazil 69

(Bray-Curtis), calculated with PASt. Abiotic factors were evaluated, with temperature and rainfall tested against carabid species richness and abundance through two multiple regressions using SPSS 16.0. Local temperature and rainfall were obtained from the 8th Meteorological District, in Porto Alegre, Rio Grande do Sul.

RESULTS

Overall 18 species and 1,733 adult carabid individuals were sampled. The highest total abundance occurred in the primary forest (747 individuals) and the lowest for Pinus silviculture (355). Secondary forest was intermediate, with 631 exemplars. Galerita lacordarei (Dejean, 1826) was the domi- Fig. 2. Individual-based rarefaction (bars are 95% CI) for carabid beetles nant species in all samples, being responsible for 72% of the among seasons, in São Francisco de Paula, southern Brazil. overall abundance. Rarefaction has shown that species richness follow the same pattern as for abundance: primary forest (14 species), environments (ANOSIM Simpson; R = 0.035; p = 0.0001; secondary forest (13 species) and Pinus silviculture (10 spe- Bray-Curtis; R = 0.070; p < 0.0001) and for seasons cies) (Fig. 1), but with significant differences only between (Simpson R = 0.122, p < 0.0001; Bray-Curtis, R = 0.196, primary forest and silviculture. There was a significantly p < 0.0001). The significant differences were between spring higher richness for summer (16 species), and winter (12 spe- and summer, as well as winter differing from all other sea- cies) was significantly richer than spring (Fig. 2). Unfortu- sons (Table I). nately a small number of traps were destroyed or lost along study. Because this, individual-based rarefaction presented has no even lines, despite effort sampling standardized. Table I. Analysis of similarity (ANOSIM) for Bray-Curtis (lower triangle) and Simpson (upper triangle) among environments for the carabid fauna, in São Francisco de Paula, southern Brazil. Transects ARA and ARB = primary forest, NEB and SEC = secondary forest, PIN and PIL = silviculture with Pinus spp. A significant value (*) means that the carabid fauna between the two compared environments are distinct. ARA ARB NEB SEC PIN PIL ARA – 0.0042* 0.0081 0 0.0004* 0.0010* ARB 0.06 – 0.5324 0.2256 0.83920.1342 NEB 0.13 0.1800 – 0.2248 0.3737 0.0973 SEC 0 0.3900 0.0500* – 0.75620.0194* PIN 0 0.2000 0.0100* 0.5000 – 0.2348 PIL 0 0 0 0.0100* 0.0300* –

Among the abiotic data there was significant influence Fig. 1. Sample-based rarefaction (error bars represent 95% CI) for carabid only for temperature on species richness, for all environments, beetles among environments in São Francisco de Paula, southern Brazil. and on abundance, but only for primary and secondary areas (Table II; Figs. 5–6). A visual inspection of the regression indicates that species richness in the primary environment The Mantel test did not show significance for the corre- was larger than expected for the observed temperatures. lation between faunal similarity and distance between sampling sites (Simpson index, correlation = -0.077; p = 0.655; Morisita index, correlation = -0.136; p = 0.761). Thus, Table II. Analysis of similarity (ANOSIM) for Bray-Curtis (lower triangle) transects in the areas were used as the scale for the analyses and Simpson (upper triangle) among climatic seasons for the carabid fauna, (n = 4, two transects in two replicates for each environment). in São Francisco de Paula, southern Brazil. A significant value (*) means There were significant differences among environments that the carabid fauna between the two compared seasons are distinct. Autumn Summer Spring Winter for abundance (MANOVA F2,152 = 17.577; p < 0.001) and Autumn – 0.9708 0.2602 0 species richness (F2,152 = 37.482; p < 0.001), however, there Summer 0.3434 – 0 0 was not for equitability (F2,152 = 2.208; p = 0.113) (Fig. 3). Seven species are common to all environments (Fig. 4). Spring 0.1533 0.0039* – 0 There were significant differences in composition both for Winter 0 0 0 –

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AB C

Fig. 3. Carabid fauna among environments in São Francisco de Paula, southern Brazil (error bars represent 95% CI). A– abundance, B– species richness and C– equitability.

DISCUSSION

Both richness and abundance followed the expected disturbance gradient: a decrease as disturbance increased. Thus, different aspects of species diversity suggest that soil carabid assemblages are distinct among environments. Causes for this distinction are probably associated to floristic composition and vegetation structure (and consequently, litter composition and structure) between the chosen environments. These factors in their turn can affect local temperature and humidity, deter- Fig. 4. Species distribution among environments for carabid beetles in São mining feeding resources and microhabitat availability Francisco de Paula, southern Brazil. Pri.: primary forests; Sec.: secondary forests; Sil.: silviculture with Pinus spp. (Barbosa et al. 2002). Our results are thus in accordance both with the disturbance response given by carabids and the response they give to habitat structure (Ganho & Marinoni 2006). Previous works also compared carabid diversity between preserved and disturbed environments (Uehara-Prado et al. 2009; Silva et al. 2008; Weller & Ganzhorn 2004), although, as here, few of them actually evaluated a gamut of habitat variables to help identify causes behind those differences in richness and abundance (Tyler 2008; Magura et al. 2003). Although carabid richness and abundance are known to be higher for undisturbed environments (Fujita et al. 2008; Magura et al. 2002), both Uehara-Prado et al. (2009) and Fernández & Costas (2004) observed higher abundance in disturbed areas. Our results do not show this increase in abun- Fig. 5. Regression between temperature and species richness for each envi- dance with disturbance. It is possible that this difference is ronment in São Francisco de Paula, southern Brazil. related to the kind of disturbance present: Uehara-Prado et al. (2009) worked with areas of Atlantic forest previously logged and burned down, transformed to pastures. They were thus open areas, not closed canopy forests as was silviculture here; open habitats perhaps can allow or induce a higher dispersal of carabids. Silva et al. (2008) evaluated carabid diversity in disturbed areas under a Mediterranean climate, identifying the most degraded environment (agriculture field under intense management) as the richer in species and showing highest abundance. This was probably due to opportunist and/or generalist species again using open spaces (sparse vegetation leading to higher mobility) and new and constant microclimatic conditions created. Also the studied region has approximately 3,000 years of intense use for agriculture, where carabid as- Fig. 6. Regression between temperature and species abundance for each semblages could even show patterns of evolutionary adapta- environment in São Francisco de Paula, southern Brazil. tion to these conditions.

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Environmental structure can define resource availability The relatively high carabid diversity and G. lacordarei for predatory arthropods. Baldissera et al. (2008) compared dominance in Pinus silviculture areas can alternatively be spider diversity in the shrub layer of exotic silviculture of Pinus attributed to its age (~30 years since planting). This has led ellioti and Eucalyptus sp. and natural forests of Araucaria to the formation of a well developed (for Pinus areas in this angustifolia, indicating the influence habitat structure can have region) shrub layer, increasing both overall environmental on predators since a higher diversity was found for Eucalyp- heterogeneity and litter diversity. Magura et al. (2003), on tus sp. areas, not the less disturbed one, but the one with more the other hand, described a low carabid diversity in exotic complex vegetation structure at the shrub level. Further stud- plantations in Hungary, even after longer periods (50 years). ies on the soil carabid fauna in the Neotropical region have Barbosa et al. (2002) suggest that beetle species exhibit much to gain from analyzing environmental variables associ- specificity towards microhabitats and thus have spatial pref- ated with litter and soil structure and heterogeneity. erences, which could be only indirectly inferred from local Apart from richness and abundance, the main effects of abundance. Certainly the species found in pine silviculture disturbance on the carabid fauna have been reported by Fujita were previously present in neighboring areas, those able to et al. (2008) as: changes in specific composition, loss of large colonize that habitat, as suggested in the similar system ex- species and those with lower dispersal abilities besides inva- plored by Magura et al. (2002). This is in accordance with sion of species from neighboring areas. A change in species Tonhasca (1994) as well: more disturbed environments would composition is a recurring observation (Uehara-Prado et al. have less resources and less complex microhabitat structure, 2009; Latty et al. 2006), since the group has a high sensibil- which would support less species but perhaps more individu- ity to environmental changes in general (Scott & Anderson als of generalist and/or opportunistic species. 2003), including canopy species (Lucky et al. 2002; Erwin A recurring difficulty in community studies involving et al. 2005). It is exactly this characteristic of carabids that carabids is how confident one can be that the recorded spe- render them good bioindicators, and it shows up in our sub- cies is closely associated with that specific local assemblage tropical Neotropical data. (Desender 1996). This hurdle is sometimes relegated and The management associated with reforestation using ex- sometimes considered in detail in the literature. Authors rel- otic species (cutting natives to open space for planted trees) egating this question to secondary status consider all species alters the carabid fauna (Magura et al. 2003). In pine planta- sampled as local, assuming that some species would have tions in Europe, one of the first consequences is the disap- low abundances, being naturally rare. Authors concerned with pearance or drastic reduction in abundance of carabids this question apply more or less random limits to which spe- specialised to those forest conditions. The new open habitats cies to consider (Desender 1996, see also Hartley et al. 2007). are thus occupied by opportunist species from any adjacent Biological knowledge can sometimes help disentangle this fields; these species were responsible for high richness and question, even though we would rarely know details about abundance levels found by Tyler (2008) in silviculture areas. the Neotropical species. Pentagonicini sp.1 and sp.2, Lebiini These carabids, however, would also tend to disappear as the sp., Rhysodhini sp. and Helluonini sp. could be considered canopy expands and closes decreasing light incidence on the vagrant species in this system, that is, species captured acci- soil surface. Generalist species are expected to persist, how- dentally whilst in a transitory environment, perhaps moving ever forest specialists would not return. In our case it seems in search of resources (Vieira 2008; Tonhasca 1994). The to differ somehow, since G. lacordarei is the dominant spe- two first morphospecies are described as arboreal and the cies in all environments, regardless of the disturbance and others as associated to fallen and/or rotting logs (as for the management history. The equitability in Pinus areas seems characteristics of the tribe, Reichardt 1977). to be higher, perhaps indicating G. lacordarei as a better com- Dominance values for both disturbed and more preserved petitor in that situation. However this is not substantiated by assemblages in our work are high, with G. lacordarei totalling the statistical analysis. 72% of all carabids sampled. It is known that few species tend The loss of large species is related to a cascade of fac- to numerically dominate carabid assemblages. For example, tors, resulting in initial dispersion when faced with manage- Latty et al. (2006) reported 61% of all individuals belonging ment radically changing the environment, and incapacity to to four common species in logged areas. Silva et al. (2008) return and/or find adequate resources once planted trees grow also found a single dominant species of carabid in a survey in (Tyler 2008; Magura et al. 2003; Magura et al. 2002). How- areas under silviculture with for exotic Eucalyptus. Invasive ever, in our case, again G. lacordarei is a large species, domi- carabid species can also be highly dominant as found by Hartley nating all areas including those under silviculture. It is clearly et al. (2007), with Pterostichus melanarius (Illiger, 1798) res- a generalist species (Thiele 1977), with high mobility (as ponsible for 80% of all individuals, followed by a rich but inferred from leg size) and probably well adapted to prevail- underrepresented native fauna. Unfortunately, there seems to ing local factors. Apparently, resources needed for this spe- be no specific studies focusing on the effects that dominant cies are homogeneously distributed (Thiele 1977) and/or species have on the assemblage. Possibly, G. lacordarei re- unknown factors are causing this. It seems probable that G. duces the available stock of resources for other species. If feed- lacordarei is very generalist and maybe also a good com- ing items are rarer, probably more dispersal is required for petitor in this assemblage. other carabids, as suggested by Paarmann et al. (2002).

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Winter is relatively rich in species, losing in richness only would favour species hibernating as larvae, since microhabi- to summer (Fig. 2). This richness in winter can be attributed to tat conditions would be more stable (Magura et al. 2002). an increase in dispersal by carabids, responding to a food short- Habitat structure can affect the way generalist predators age (mainly the dominant herbivores). A higher mobility would find and hunt their prey. Analysing the spider fauna from the lead to high captures by the pitfalls. Different abiotic factors same pitfall trapping samples of the present study, Ott (2004) can thus influence the activity of carabid beetles and associa- found differences in spider abundance only between silvi- ted taxa in different climates. Among these factors, tempera- culture areas and the other two types of forests. As regards ture had a strong influence on richness, contrary to what spider richness, all three environments were distinct, with Paarmann et al. (1998) found, in which rainfall was decisive primary areas richer than secondary, and those two richer for variation in the assemblages of cicindeline beetles in the than silviculture. Although these are different groups of preda- Amazon. This sort of difference has been attributed to the af- tory soil arthropods, with potentially many shared prey, both finity and adaptation by local species to their habitats (Erwin resource and resource use might differ qualitative and quan- et al. 2005). Soil humidity is reported as an important charac- titatively. Whilst spiders can be grouped in rather clear re- teristic for carabid beetles (Lövei & Sunderland 1996), but source exploration guilds, Neotropical soil carabid species our results do not show any relation to rainfall (Table III). Ei- are virtually unknown in terms of resource use. For some ther this assemblage responds to humidity in a subtler way, or groups, what seems to be important for functional distinc- else the constant rainfall in this region never leads to low le- tion among species is: (1) division of prey, with relative vels of soil humidity (especially in areas covered by forests). specialisation (Straneo & Ball 1989; Erwin & Erwin 1976), (2) the inclusion of frugivory, (Marinoni et al. 2001; Paarmann et al. 2001), (3) shared exploration of environ- Table III. Multiple regressions between abiotic factors (temperature and mental characteristics (Schreiner & Irmler 2009) and of the rainfall) and diversity variables (species richness and abundance) of the leaf litter (Loreau 1987), (4) differing biotic and abiotic re- carabid fauna for each studied environment in São Francisco de Paula, southern Brazil. Significant differences are marked with asterisks. quirements for reproduction (Thiele 1977). 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Received 14 July 2011; accepted 05 November 2012 Associate Editor: Lúcia M. Almeida

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